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Timing deficits in attention-deficit/hyperactivity disorder (ADHD): Evidence from neurocognitive and neuroimaging studies
Open accessAbstract
Relatively recently, neurocognitive and neuroimaging studies have indicated that individuals with attention-deficit/hyperactivity disorder (ADHD) may have deficits in a range of timing functions and their underlying neural networks. Despite this evidence, timing deficits in ADHD are still somewhat neglected in the literature and mostly omitted from reviews on ADHD. There is therefore a lack of integrative reviews on the up-to-date evidence on neurocognitive and neurofunctional deficits of timing in ADHD and their significance with respect to other behavioural and cognitive deficits. The present review provides a synthetic overview of the evidence for neurocognitive and neurofunctional deficits in ADHD in timing functions, and integrates this evidence with the cognitive neuroscience literature of the neural substrates of timing. The review demonstrates that ADHD patients are consistently impaired in three major timing domains, in motor timing, perceptual timing and temporal foresight, comprising several timeframes spanning milliseconds, seconds, minutes and longer intervals up to years. The most consistent impairments in ADHD are found in sensorimotor synchronisation, duration discrimination, reproduction and delay discounting. These neurocognitive findings of timing deficits in ADHD are furthermore supported by functional neuroimaging studies that show dysfunctions in the key inferior fronto-striato-cerebellar and fronto-parietal networks that mediate the timing functions. Although there is evidence that these timing functions are inter-correlated with other executive functions that are well established to be impaired in the disorder, in particular working memory, attention, and to a lesser degree inhibitory control, the key timing deficits appear to survive when these functions are controlled for, suggesting independent cognitive deficits in the temporal domain. There is furthermore strong evidence for an association between timing deficits and behavioural measures of impulsiveness and inattention, suggesting that timing problems are key to the clinical behavioural profile of ADHD. Emerging evidence shows that the most common treatment of ADHD with the dopamine agonist and psychostimulant Methylphenidate attenuates most timing deficits in ADHD and normalises the abnormally blunted recruitment of the underlying fronto-striato-cerebellar networks. Timing function deficits in ADHD, therefore, next to executive function deficits, form an independent impairment domain, and should receive more attention in neuropsychological, neuroimaging, and pharmacological basic research as well as in translational research aimed to develop pharmacological or non-pharmacological treatment of abnormal timing behaviour and cognition in ADHD.
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“as well as in temporal processing (i.e., motor timing, time estimation and temporal foresight), with most consistent deficits in time discrimination and estimation tasks (Rubia et al., 2009a; Noreika et al., 2013).”
From Cognitive Neuroscience of Attention Deficit Hyperactivity Disorder (ADHD) and Its Clinical Translation (2018) · cites this paper as Noreika et al., 2013
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“accumulating evidence indicates that timing functions are impaired in a variety of developmental disorders including ADHD [32,33], dyslexia [34], and autism [35,36].”
From The Conceptual and Methodological Mayhem of “Screen Time” (2020) · cites this paper as [33]
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“However, impairment has also been found in so-called “hot” EF functions of motivation control and reward-related decision making, as measured in temporal discounting and gambling tasks, with, however, more inconsistent findings (Willcutt et al., 2008; Noreika et al., 2013; Plichta and Scheres, 2014).”
From Cognitive Neuroscience of Attention Deficit Hyperactivity Disorder (ADHD) and Its Clinical Translation (2018) · cites this paper as Noreika et al., 2013
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“Few studies have measured brain response to delay discounting tasks, which are impaired in ADHD, with, however, also some negative findings (Noreika et al., 2013).”
From Cognitive Neuroscience of Attention Deficit Hyperactivity Disorder (ADHD) and Its Clinical Translation (2018) · cites this paper as Noreika et al., 2013
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“Attention-deficit/hyperactivity disorder is associated with inhibition, attention, working memory (WM), and timing deficits 2, 3, 4, 5”
From Effects of stimulants on brain function in attention-deficit/hyperactivity disorder: a systematic review and meta-analysis (2014) · cites this paper as [5]
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Time Processing, Interoception, and Insula Activation: A Mini-Review on Clinical Disorders
Vicario, C. M., Nitsche, M. A., Salehinejad, M. A., Avanzino, L., & Martino, G. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.01893 · Cited by 46
Voon, V., & Dalley, J. W. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_5013 · Cited by 46
“In humans, delay discounting is a core impairment implicated in ADHD (Noreika et al. 2013) and substance addictions across multiple drug categories, pathological gambling (Bickel et al.”
BackgroundHart, H. C., Marquand, A. F., Smith, A. B., Cubillo, A., Simmons, A., Brammer, M. J., & Rubia, K. (2014) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2013.12.024 · Cited by 45
Self-citationCortese, S., Castellanos, F. X., Eickhoff, C. R., D’Acunto, G., Masi, G., Fox, P. T., Laird, A. R., & Eickhoff, S. B. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.06.014 · Cited by 43
“(60), individuals with ADHD have been found to present multiple deficits in timing functions, including motor timing (estimated with tasks of free tapping, sensorimotor synchronization, and rhythm reproduction), perceptual timing (assessed using tasks of duration discrimination, verbal duration estimation, and duratio…”
BackgroundTiming Deficits in ADHD: Insights From the Neuroscience of Musical Rhythm
Slater, J., & Tate, M. C. (2018) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2018.00051 · Cited by 54
“We have chosen to consider ADHD in particular because in addition to the core symptoms of inattention and/or hyperactivity/impulsivity, ADHD is also characterized by deficits in motor and perceptual timing (Smith et al., 2002; Fair et al., 2012; Zelaznik et al., 2012; Demers et al., 2013; Noreika et al., 2013).”
BackgroundMethodOrtiz, N., Parsons, A., Whelan, R., Brennan, K., Agan, M., O'Connell, R., Bramham, J., & Garavan, H. (2015) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-2015-2038 · Cited by 40
“Previous studies have shown that persons with ADHD have deficits in motor and perceptual timing functions that are dependent on cerebellar activation (Noreika et al. 2013).”
BackgroundTask-Based Functional Connectivity in Attention-Deficit/Hyperactivity Disorder: A Systematic Review
Kowalczyk, O. S., Mehta, M. A., O’Daly, O., & Criaud, M. (2021) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2021.10.006 · Cited by 44
Murphy, C. M., Christakou, A., Giampietro, V., Brammer, M. J., Daly, E., Ecker, C., Johnston, P., Spain, D., Robertson, D., Murphy, D., et al. (2017) · Human Brain Mapping · doi:10.1002/hbm.23718 · Cited by 39
“…discounting tasks typically measure the choice between a small immediate or a larger delayed reward and require both inhibition of immediate reward and temporal foresight (forward thinking/future consideration of current choice) to choose the delayed reward (Rubia et al. 2009, Noreika et al. 2013).”
Self-citationInteroceptive awareness in patients with attention-deficit/hyperactivity disorder (ADHD)
Kutscheidt, K., Dresler, T., Hudak, J., Barth, B., Blume, F., Ethofer, T., Fallgatter, A. J., & Ehlis, A. (2019) · ADHD Attention Deficit and Hyperactivity Disorders · doi:10.1007/s12402-019-00299-3 · Cited by 50
Anterior insula hyperactivation in ADHD when faced with distracting negative stimuli
Vetter, N. C., Buse, J., Backhausen, L. L., Rubia, K., Smolka, M. N., & Roessner, V. (2018) · Human Brain Mapping · doi:10.1002/hbm.24053 · Cited by 41
Self-citationMartín-Moratinos, M., Bella-Fernández, M., & Blasco-Fontecilla, H. (2023) · Journal of Medical Internet Research · doi:10.2196/37742 · Cited by 40
“…or rhythm reproduction task), perceptual timing (eg, with a discrimination task, verbal duration estimation, or a duration production or reproduction task), and temporal foresight (eg, with major difficulty to work it through delay or temporal discounting or gambling paradigms) [18].”
InfluentialLong-term impact of digital media on brain development in children
Nivins, S., Sauce, B., Liebherr, M., Judd, N., & Klingberg, T. (2024) · Scientific Reports · doi:10.1038/s41598-024-63566-y · Cited by 51
Mioni, G., Santon, S., Stablum, F., & Cornoldi, C. (2016) · Child Neuropsychology · doi:10.1080/09297049.2016.1172561 · Cited by 40
“The authors suggested that good candidates for explaining the lower PM accuracy of children with ADHD included deficits in time estimation (Noreika et al., 2013) and working memory (McInnes et al.”
BackgroundResultInfluentialCognitive mechanisms underlying depressive disorders in ADHD: A systematic review
Mayer, J. S., Bernhard, A., Fann, N., Boxhoorn, S., Hartman, C. A., Reif, A., & Freitag, C. M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.12.018 · Cited by 48
Reduced pain perception in children and adolescents with ADHD is normalized by methylphenidate
Wolff, N., Rubia, K., Knopf, H., Hölling, H., Martini, J., Ehrlich, S., & Roessner, V. (2016) · Child and Adolescent Psychiatry and Mental Health · doi:10.1186/s13034-016-0112-9 · Cited by 35
Self-citationIsfandnia, F., El Masri, S., Radua, J., & Rubia, K. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105703 · Cited by 36
Self-citationBégel, V., Seilles, A., & Bella, S. D. (2018) · Music & Science · doi:10.1177/2059204318794369 · Cited by 49
Cory‐Slechta, D. A., Sobolewski, M., & Oberdörster, G. (2020) · Atmosphere · doi:10.3390/atmos11101098 · Cited by 36
Selective Attention and Inhibitory Control of Attention Are Correlated With Music Audiation
Grinspun, N., Nijs, L., Kausel, L., Onderdijk, K. E., Sepúlveda, N., & Rivera-Hutinel, A. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.01109 · Cited by 44
Bella, S. D., & Sowiński, J. (2015) · Journal of Visualized Experiments · doi:10.3791/51761 · Cited by 47
Mueller, A. K., Tucha, L., Koerts, J., Groen, Y., Lange, K. W., & Tucha, O. M. (2014) · Journal of Molecular Psychiatry · doi:10.1186/2049-9256-2-5 · Cited by 40
“It has been hypothesized that a decreased processing speed might lead to a general distortion in individuals’ perception of time [58] and impacts on several timing functions such as motor- and perceptual timing, as well as temporal foresight [63].”
BackgroundNorman, L. J., Carlisi, C. O., Christakou, A., Chantiluke, K. C., Murphy, C. M., Simmons, A., Giampietro, V., Brammer, M. J., Mataix‐Cols, D., & Rubia, K. (2017) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2017.09.008 · Cited by 35
“…of time in units of reward (delay aversion), temporal foresight to understand the future gain of the delayed choice, as well as inter-temporal decision making and reward evaluation with respect to its delay (Christakou et al., 2011; Hamilton et al., 2015; Noreika et al., 2013; Rubia et al., 2009).”
InfluentialSelf-citationSchweren, L., Hoekstra, P. J., van Lieshout, M., Oosterlaan, J., Rommelse, N. N. J., Buitelaar, J. K., Franke, B., & Hartman, C. A. (2018) · Psychological Medicine · doi:10.1017/s0033291718000545 · Cited by 39
“ADHD has been associated with a broad range of neurocognitive deficits, including impaired executive functioning (Willcutt et al. 2005), timing deficits (Noreika et al. 2013) and higher response time variability (Klein et al. 2006).”
BackgroundHyun, G. J., Jung, T.-W., Park, J. H., Kang, K. D., Kim, S. M., Son, Y., Cheong, J. H., Kim, B.-N., & Han, D. H. (2016) · The Journal of Alternative and Complementary Medicine · doi:10.1089/acm.2015.0299 · Cited by 35
Music and movement: Towards a translational approach
Bella, S. D. (2018) · Neurophysiologie Clinique · doi:10.1016/j.neucli.2018.10.067 · Cited by 44
Pranjić, M., Rahman, N., Kamenetskiy, A., Mulligan, K., Pihl, S., & Arnett, A. B. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105389 · Cited by 43
Vogel, D. H. V., Falter‐Wagner, C. M., Schoofs, T., Krämer, K., Kupke, C., & Vogeley, K. T. (2018) · Phenomenology and the Cognitive Sciences · doi:10.1007/s11097-018-9573-z · Cited by 33
Inferior Auditory Time Perception in Children With Motor Difficulties
Chang, A., Li, Y., Chan, J. F., Dotov, D. G., Cairney, J., & Trainor, L. J. (2021) · Child Development · doi:10.1111/cdev.13537 · Cited by 35
Risky bicycling behavior among youth with and without attention‐deficit hyperactivity disorder
Nikolas, M. A., Elmore, A. L., Franzen, L., O’Neal, E. E., Kearney, J. K., & Plumert, J. M. (2015) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12491 · Cited by 32
The effects of acute fluoxetine administration on temporal discounting in youth with ADHD
Carlisi, C. O., Chantiluke, K. C., Norman, L. J., Christakou, A., Barrett, N., Giampietro, V., Brammer, M. J., Simmons, A., & Rubia, K. (2015) · Psychological Medicine · doi:10.1017/s0033291715002731 · Cited by 31
“TD matures with age (Christakou et al. 2011) and varies between individuals, with steeper TD, i.e. more rapidly decaying rates of reward discounting with increasing time (Richards et al. 1999), in more impulsive subjects (Rubia et al. 2009; Noreika et al. 2013).”
BackgroundInfluentialSelf-citationWennberg, B., Janeslätt, G. K., Kjellberg, A., & Gustafsson, P. A. (2017) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-017-1052-5 · Cited by 43
“[11] state in a review that persons with ADHD have timing deficits in motor timing, time estimation and temporal foresight.”
BackgroundKhoshnoud, S., Shamsi, M., Nazari, M. A., & Makeig, S. (2017) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803395.2017.1406897 · Cited by 30
“…synchronization in a range of seconds seems to be mediated more by the prefrontal cortex, especially the DLPFC, whereas in a range of milliseconds it is associated with activation in the midfrontal brain, particularly the SMA (Noreika et al., 2013; Rubia et al., 2009; Smith et al., 2008).”
BackgroundResultInfluentialA time-based intervention to treat impulsivity in male and female rats
Panfil, K., Bailey, C., Davis, I. R., Mains, A., & Kirkpatrick, K. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112316 · Cited by 31
Ghaderyan, P., Moghaddam, F., Khoshnoud, S., & Shamsi, M. (2022) · Measurement · doi:10.1016/j.measurement.2022.111468 · Cited by 30
Duff, C. T., & Sulla, E. M. (2015) · Applied Neuropsychology: Child · doi:10.1080/21622965.2013.848329 · Cited by 28
Wiggs, K. K., Elmore, A. L., Nigg, J. T., & Nikolas, M. A. (2016) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-016-0142-z · Cited by 31
“…and Tannock 2006), memory span, response inhibition (Barkley 1997), processing speed, response variability (Karalunas et al. 2014), temporal processing (Noreika et al. 2013; Toplak and Tannock 2005), and arousal (or activation; operationalized as signal detection sensitivity; Sergeant 2005).”
BackgroundSystematic overview of neuroanatomical differences in ADHD: Definitive evidence
de Melo, B. B. V., Trigueiro, M. J., & Rodrigues, P. P. (2017) · Developmental Neuropsychology · doi:10.1080/87565641.2017.1414821 · Cited by 32
Salunkhe, G., Weissbrodt, K., Feige, B., Saville, C. W. N., Berger, A., Dundon, N. M., Bender, S., Smyrnis, N., Beauducel, A., Biscaldi, M., et al. (2018) · Journal of Attention Disorders · doi:10.1177/1087054718778114 · Cited by 31
Metadata
- Authors
- Noreika, V., Falter, C. M., & Rubia, K.
- Affiliations
- University of Turku (FI)
- University of Groningen (NL)
- King's College London (GB)
- Corresponding author
- Noreika, Valdas
- Venue
- Neuropsychologia
- Publisher
- Elsevier BV
- Published
- 2013-01
- Volume
- 51
- Issue
- 2
- Pages
- 235-266
- ISSN
- 0028-3932 (ISSN-L)
- OpenAlex
- W2136109876
- Semantic Scholar
- 91baa62bc9566578be57372069278ef520b7ae43
- Cited by
- 339
- References
- 246
- Citations by year
- 2026: 23 · 2025: 19 · 2024: 21 · 2023: 24 · 2022: 26 · 2021: 33 · 2020: 27 · 2019: 23 · 2018: 30 · 2017: 24 · 2016: 28 · 2015: 22 · 2014: 21 · 2013: 16
- FWCI
- 13.93
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- Neuropsychologia (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- Research Portal (King's College London) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Funders
- European Cooperation in Science and Technology (COST) action on Time in Mental Activity (TIMELY, TD0904)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Attention Deficit Hyperactivity Disorder
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Keywords
- attention deficit hyperactivity disorder, timing deficits, temporal processing, duration discrimination, delay discounting, frontoparietal network, executive function, working memory, impulsivity, inattention, methylphenidate, dopamine agonists
- MeSH terms
- Attention Deficit Disorder with Hyperactivity, Female, Humans, Male, Neuropsychological Tests, Perceptual Disorders, Time Perception, Neuroimaging
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